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Applied and Environmental Microbiology, March 2004, p. 1698-1707, Vol. 70, No. 3
0099-2240/04/$08.00+0     DOI: 10.1128/AEM.70.3.1698-1707.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Molecular Evidence for the Evolution of Metal Homeostasis Genes by Lateral Gene Transfer in Bacteria from the Deep Terrestrial Subsurface

J. M. Coombs and T. Barkay*

Department of Biochemistry and Microbiology, Cook College, Rutgers University, New Brunswick, New Jersey 08901

Received 18 August 2003/ Accepted 27 November 2003

Lateral gene transfer (LGT) plays a vital role in increasing the genetic diversity of microorganisms and promoting the spread of fitness-enhancing phenotypes throughout microbial communities. To date, LGT has been investigated in surface soils, natural waters, and biofilm communities but not in the deep terrestrial subsurface. Here we used a combination of molecular analyses to investigate the role of LGT in the evolution of metal homeostasis in lead-resistant subsurface bacteria. A nested PCR approach was employed to obtain DNA sequences encoding PIB-type ATPases, which are proteins that transport toxic or essential soft metals such as Zn(II), Cd(II), and Pb(II) through the cell wall. Phylogenetic incongruencies between a 16S rRNA gene tree and a tree based on 48 PIB-type ATPase amplicons and sequences available for complete bacterial genomes revealed an ancient transfer from a member of the ß subclass of the Proteobacteria (ß-proteobacterium) that may have predated the diversification of the genus Pseudomonas. Four additional phylogenetic incongruencies indicate that LGT has occurred among groups of ß- and {gamma}-proteobacteria. Two of these transfers appeared to be recent, as indicated by an unusual G+C content of the PIB-type ATPase amplicons. This finding provides evidence that LGT plays a distinct role in the evolution of metal homeostasis in deep subsurface bacteria, and it shows that molecular evolutionary approaches may be used for investigation of this process in microbial communities in specific environments.


* Corresponding author. Mailing address: Department of Biochemistry and Microbiology, 76 Lipman Dr., New Brunswick, NJ 08901. Phone: (732) 932-9763, ext. 333. Fax: (732) 932-8965. E-mail: barkay{at}aesop.rutgers.edu.


Applied and Environmental Microbiology, March 2004, p. 1698-1707, Vol. 70, No. 3
0099-2240/04/$08.00+0     DOI: 10.1128/AEM.70.3.1698-1707.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.




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